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      The Association Between Inflammaging and Age-Related Changes in the Ruminal and Fecal Microbiota Among Lactating Holstein Cows

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          Abstract

          Inflammaging is well understood in the study of humans; however, it is rarely reported for dairy cows. To understand the changing pattern of the gut microbiota, inflammatory status and milk production performance during the aging process in cows, we grouped 180 cows according to their lactation period: L1 ( n = 60, 1st lactation), L3 ( n = 60, 3rd lactation), and L5+ ( n = 60, at least 5th lactation) and analyzed their milk components and daily milk yields to evaluate the changing pattern of milk production. The microbiota was analyzed using high-throughput sequencing of amplicons of 16S rRNA, which also allowed us to predict the functions of microbes and then study the changing pattern of the ruminal and fecal microbiota. Serum cytokines, including TNF-α, IL-6, IL-10, and TGF-β were measured to study the progress of inflammaging in the cows. We found that old cows (L5+) suffered from a long-term and low-level chronic inflammation, as indicated by significantly higher levels of inflammatory cytokines IL-10, TNF-α, and TGF-β in the L5+ group ( p < 0.001). We also observed a significant decrease in daily milk yield and milk lactose, as well as a significant increase in somatic cell score, among the cows in the L5+ group. For the gut microbiota, most of the genera belonging to Prevotellaceae and Lachnospiraceae, which had a higher abundance among cows of both the L1 and L3 groups (LEfSe, LDA > 2), showed a similar change pattern during the aging process, both in the rumen and in feces, and across the six farms. Beneficial bacteria, like Bacteroidaceae, Eubacterium, and Bifidobacterium, displayed lower abundance in the feces of the L5+ group (LEfSe, LDA > 2). Reconstruction of the fecal bacteria community indicated transformation of the fermenting pattern of older cows’ (L5+) feces microbiota, with increased functions related the protein metabolism and fewer functions related to carbohydrate and lipid metabolism compared with those in L1 ( p < 0.05). Finally, the connections among these changing patterns were revealed using redundancy analysis and network analysis. The results support the hypothesis of prolonging a cows’ productive life and improve dairy cow milk productive performances by manipulating the gut microbiota.

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          Most cited references21

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          The microbiome and innate immunity.

          The intestinal microbiome is a signalling hub that integrates environmental inputs, such as diet, with genetic and immune signals to affect the host's metabolism, immunity and response to infection. The haematopoietic and non-haematopoietic cells of the innate immune system are located strategically at the host-microbiome interface. These cells have the ability to sense microorganisms or their metabolic products and to translate the signals into host physiological responses and the regulation of microbial ecology. Aberrations in the communication between the innate immune system and the gut microbiota might contribute to complex diseases.
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            Through Ageing, and Beyond: Gut Microbiota and Inflammatory Status in Seniors and Centenarians

            Background Age-related physiological changes in the gastrointestinal tract, as well as modifications in lifestyle, nutritional behaviour, and functionality of the host immune system, inevitably affect the gut microbiota, resulting in a greater susceptibility to infections. Methodology/Principal Findings By using the Human Intestinal Tract Chip (HITChip) and quantitative PCR of 16S rRNA genes of Bacteria and Archaea, we explored the age-related differences in the gut microbiota composition among young adults, elderly, and centenarians, i.e subjects who reached the extreme limits of the human lifespan, living for over 100 years. We observed that the microbial composition and diversity of the gut ecosystem of young adults and seventy-years old people is highly similar but differs significantly from that of the centenarians. After 100 years of symbiotic association with the human host, the microbiota is characterized by a rearrangement in the Firmicutes population and an enrichment in facultative anaerobes, notably pathobionts. The presence of such a compromised microbiota in the centenarians is associated with an increased inflammatory status, also known as inflammageing, as determined by a range of peripheral blood inflammatory markers. This may be explained by a remodelling of the centenarians' microbiota, with a marked decrease in Faecalibacterium prauznitzii and relatives, symbiotic species with reported anti-inflammatory properties. As signature bacteria of the long life we identified specifically Eubacterium limosum and relatives that were more than ten-fold increased in the centenarians. Conclusions/Significance We provide evidence for the fact that the ageing process deeply affects the structure of the human gut microbiota, as well as its homeostasis with the host's immune system. Because of its crucial role in the host physiology and health status, age-related differences in the gut microbiota composition may be related to the progression of diseases and frailty in the elderly population.
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              Inflammaging as a major characteristic of old people: can it be prevented or cured?

              Widespread aging at the population level is a recent phenomenon that emerged in affluent societies. Inflammation is necessary to cope with damaging agents and is crucial for survival, particularly to cope with acute inflammation during our reproductive years. But chronic exposure to a variety of antigens, especially to some viruses such as cytomegalovirus, for a period much longer than that predicted by evolution, induces a chronic low-grade inflammatory status that contributes to age-associated morbidity and mortality. This condition carries the proposed name "inflammaging". Centenarians are unique in that, despite high levels of pro-inflammatory markers, they also exhibit anti-inflammatory markers that may delay disease onset. The key to successful aging and longevity is to decrease chronic inflammation without compromising an acute response when exposed to pathogens.
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                Author and article information

                Contributors
                Journal
                Front Microbiol
                Front Microbiol
                Front. Microbiol.
                Frontiers in Microbiology
                Frontiers Media S.A.
                1664-302X
                09 August 2019
                2019
                : 10
                : 1803
                Affiliations
                [1] 1Key Laboratory of Animal Genetics, Breeding and Reproduction, Ministry of Agriculture and Rural Affairs, National Engineering Laboratory for Animal Breeding, College of Animal Science and Technology, China Agricultural University , Beijing, China
                [2] 2Shenzhen Weishengtai Technology Co., Ltd. , Shenzhen, China
                [3] 3College of Life Sciences and Bioengineering, Beijing Jiaotong University , Beijing, China
                [4] 4State Key Laboratory of Animal Nutrition, College of Animal Science and Technology, China Agricultural University , Beijing, China
                [5] 5Beijing Sunlon Livestock Development Co., Ltd. , Beijing, China
                Author notes

                Edited by: Garret Suen, University of Wisconsin−Madison, United States

                Reviewed by: Naoki Fukuma, Obihiro University of Agriculture and Veterinary Medicine, Japan; Nilusha Malmuthuge, University of Alberta, Canada

                *Correspondence: Yachun Wang, wangyachun@ 123456cau.edu.cn

                This article was submitted to Systems Microbiology, a section of the journal Frontiers in Microbiology

                Article
                10.3389/fmicb.2019.01803
                6696898
                31447814
                e02a20e7-2a96-4356-b5f9-823c82a9c294
                Copyright © 2019 Zhang, Wang, Luo, Qiu, Zhang, Hu, Wang, Dong and Guo.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 24 March 2019
                : 22 July 2019
                Page count
                Figures: 8, Tables: 4, Equations: 0, References: 47, Pages: 17, Words: 0
                Funding
                Funded by: Agriculture Research System of China 10.13039/501100010203
                Categories
                Microbiology
                Original Research

                Microbiology & Virology
                inflammatory cytokines,gut microbiota,inflammaging,16s rrna,metagenome
                Microbiology & Virology
                inflammatory cytokines, gut microbiota, inflammaging, 16s rrna, metagenome

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